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PMID: 9275197 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast.

Datta A, Hendrix M, Lipsitch M, Jinks-Robertson S

Abstract

Sequence divergence acts as a potent barrier to homologous recombination; much of this barrier derives from an antirecombination activity exerted by mismatch repair proteins. An inverted repeat assay system with recombination substrates ranging in identity from 74% to 100% has been used to define the relationship between sequence divergence and the rate of mitotic crossing-over in yeast. To elucidate the role of the mismatch repair machinery in regulating recombination between mismatched substrates, we performed experiments in both wild-type and mismatch repair defective strains. We find that a single mismatch is sufficient to inhibit recombination between otherwise identical sequences, and that this inhibition is dependent on the mismatch repair system. Additional mismatches have a cumulative negative effect on the recombination rate. With sequence divergence of up to approximately 10%, the inhibitory effect of mismatches results mainly from antirecombination activity of the mismatch repair system. With greater levels of divergence, recombination is inefficient even in the absence of mismatch repair activity. In both wild-type and mismatch repair defective strains, an approximate log-linear relationship is observed between the recombination rate and the level of sequence divergence.

MeSH Terms
Crossing Over, Genetic DNA Repair DNA, Fungal/genetics Recombination, Genetic Saccharomyces cerevisiae/genetics
Chemicals
DNA, Fungal
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Datta A
Department of Biology, Emory University, Atlanta, GA 30322, USA.
Hendrix M
Lipsitch M
Jinks-Robertson S
References (39)
39 references, click to expand
  1. Differential effects of base-pair mismatch on intrachromosomal versus extrachromosomal recombination in mouse cells.
    Proc Natl Acad Sci U S A. 1987 Aug;84(15):5340-4 PMID: 3037544
  2. Homology requirement for efficient gene conversion between duplicated chromosomal sequences in mammalian cells.
    Genetics. 1987 Jan;115(1):161-7 PMID: 3557108
  3. Improved method for high efficiency transformation of intact yeast cells.
    Nucleic Acids Res. 1992 Mar 25;20(6):1425 PMID: 1561104
  4. Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species.
    Cell. 1995 Feb 10;80(3):507-15 PMID: 7859291
  5. Getting started with yeast.
    Methods Enzymol. 1991;194:3-21 PMID: 2005794
  6. The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust.
    Genetics. 1995 Jul;140(3):917-32 PMID: 7672591
  7. The distribution of the numbers of mutants in bacterial populations.
    J Genet. 1949 Dec;49(3):264-85 PMID: 24536673
  8. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae.
    Genetics. 1995 Mar;139(3):1175-88 PMID: 7768431
  9. Biochemistry and genetics of eukaryotic mismatch repair.
    Genes Dev. 1996 Jun 15;10(12):1433-42 PMID: 8666228
  10. Sequence and expression of the chicken beta 3 tubulin gene. A vertebrate testis beta-tubulin isotype.
    J Biol Chem. 1986 Oct 5;261(28):13317-22 PMID: 3759966
  11. Apparent gene conversion between beta-tubulin genes yields multiple regulatory pathways for a single beta-tubulin polypeptide isotype.
    Mol Cell Biol. 1985 Sep;5(9):2454-65 PMID: 3837190
  12. Inactivation of mismatch repair overcomes the barrier to transduction between Salmonella typhimurium and Salmonella typhi.
    J Bacteriol. 1994 Mar;176(5):1527-9 PMID: 8113197
  13. Control of large chromosomal duplications in Escherichia coli by the mismatch repair system.
    Genetics. 1991 Oct;129(2):327-32 PMID: 1743481
  14. DNA-replication fidelity, mismatch repair and genome instability in cancer cells.
    Eur J Biochem. 1996 Jun 1;238(2):297-307 PMID: 8681938
  15. Effect of base pair mismatches on recombination via the RecBCD pathway.
    Mol Gen Genet. 1989 Aug;218(2):358-60 PMID: 2550771
  16. Distance-independence of mitotic intrachromosomal recombination in Saccharomyces cerevisiae.
    Genetics. 1990 Feb;124(2):263-73 PMID: 2407612
  17. Homologous and homeologous intermolecular gene conversion are not differentially affected by mutations in the DNA damage or the mismatch repair genes RAD1, RAD50, RAD51, RAD52, RAD54, PMS1 and MSH2.
    Genetics. 1996 Jun;143(2):755-67 PMID: 8725224
  18. Homologous recombination between the tuf genes of Salmonella typhimurium.
    J Mol Biol. 1996 Jul 26;260(4):506-22 PMID: 8759317
  19. Destabilization of simple repetitive DNA sequences by transcription in yeast.
    Genetics. 1996 Jun;143(2):713-21 PMID: 8725221
  20. Effect of limited homology on gene conversion in a Saccharomyces cerevisiae plasmid recombination system.
    Mol Cell Biol. 1988 Jun;8(6):2442-8 PMID: 3043177
  21. Sequence of chicken c beta 7 tubulin. Analysis of a complete set of vertebrate beta-tubulin isotypes.
    J Mol Biol. 1988 Feb 5;199(3):439-46 PMID: 3351937
  22. The mismatch repair system reduces meiotic homeologous recombination and stimulates recombination-dependent chromosome loss.
    Mol Cell Biol. 1996 Nov;16(11):6110-20 PMID: 8887641
  23. Determination of the amount of homology required for recombination in bacteriophage T4.
    Cell. 1982 Nov;31(1):25-33 PMID: 6297750
  24. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer.
    Cell. 1995 Jul 28;82(2):321-30 PMID: 7628020
  25. Genetic recombination in E. coli: RuvC protein cleaves Holliday junctions at resolution hotspots in vitro.
    Cell. 1994 Dec 2;79(5):853-64 PMID: 8001122
  26. The minimum amount of homology required for homologous recombination in mammalian cells.
    Mol Cell Biol. 1984 Nov;4(11):2253-8 PMID: 6096689
  27. Requirement of mismatch repair genes MSH2 and MSH3 in the RAD1-RAD10 pathway of mitotic recombination in Saccharomyces cerevisiae.
    Genetics. 1996 Mar;142(3):727-36 PMID: 8849883
  28. Repair of specific base pair mismatches formed during meiotic recombination in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1991 Feb;11(2):737-45 PMID: 1990280
  29. Homeologous recombination and mismatch repair during transformation in Streptococcus pneumoniae: saturation of the Hex mismatch repair system.
    Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9052-6 PMID: 7568071
  30. Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3238-41 PMID: 8159731
  31. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccaromyces cerevisiae.
    Mol Cell Biol. 1996 Mar;16(3):1085-93 PMID: 8622653
  32. The sequence and expression of the divergent beta-tubulin in chicken erythrocytes.
    J Biol Chem. 1987 Oct 15;262(29):14305-12 PMID: 2888766
  33. Gene conversions and crossing over during homologous and homeologous ectopic recombination in Saccharomyces cerevisiae.
    Genetics. 1993 Sep;135(1):5-16 PMID: 8224827
  34. Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Jul;13(7):3937-50 PMID: 8321201
  35. Homologous recombination in Escherichia coli: dependence on substrate length and homology.
    Genetics. 1986 Mar;112(3):441-57 PMID: 3007275
  36. Influence of DNA sequence identity on efficiency of targeted gene replacement.
    Mol Cell Biol. 1997 Jan;17(1):278-86 PMID: 8972208
  37. Mismatch repair in replication fidelity, genetic recombination, and cancer biology.
    Annu Rev Biochem. 1996;65:101-33 PMID: 8811176
  38. Altered replication and inverted repeats induce mismatch repair-independent recombination between highly diverged DNAs in yeast.
    Mol Cell Biol. 1997 Feb;17(2):1027-36 PMID: 9001255
  39. Avoidance of inter-repeat recombination by sequence divergence and a mechanism of neutral evolution.
    Biochimie. 1991 Apr;73(4):357-61 PMID: 1911937
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-09-02
Pages
9757-62
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC23263
Subset
IM
Grants
NIGMS NIH HHS · R01 GM033782 · United States
NIGMS NIH HHS · R01 GM038464 · United States
NIGMS NIH HHS · GM33782 · United States
NIGMS NIH HHS · GM38464 · United States
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